Modulation of parasympathetic neuron phenotype and function by sympathetic innervation

Smith, Peter G.; Warn, J. D.; Steinle, Jena J.; Krizsan-Agbas, Dora; Hasan, Wohaib

doi:10.1016/s1566-0702(01)00371-x

Cited by 22 publications

(25 citation statements)

References 61 publications

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“…These intercellular factors contribute to selective synaptic maturation and elimination during the development of functional neural circuits. Several factors are also implicated in the consolidation and pruning of distinct subsets of synapses depending on neural activity (English and Schwartz, 1995;Smith et al, 2002). The present results showed that ErbB1 receptor ligands act as a negative regulator for the expression and accumulation of PDZ proteins and that they might be involve in selective synaptic development or elimination.…”

Section: Positive and Negative Regulation Of Pdz Protein Expression Amentioning

confidence: 50%

“…Treatment of primary cortical neurons with bFGF selectively down-regulated protein expression of the PDZ proteins and decreased their interaction to AMPAR (Jourdi and Nawa, 2002). The concept of selective neural connections was introduced in the classic studies on the development of neuromuscular synapses or on the innervation of the superior cervical ganglion (English and Schwartz, 1995;Smith et al, 2002). These intercellular factors contribute to selective synaptic maturation and elimination during the development of functional neural circuits.…”

Section: Positive and Negative Regulation Of Pdz Protein Expression Amentioning

confidence: 99%

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ErbB1 receptor ligands attenuate the expression of synaptic scaffolding proteins, GRIP1 and SAP97, in developing neocortex

Yokomaku¹,

Jourdi²,

Kakita³

et al. 2005

Neuroscience

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Scaffolding proteins containing postsynaptic density-95/discs large/zone occludens-1 (PDZ) domains interact with synaptic receptors and cytoskeletal components and are therefore implicated in synaptic development and plasticity. Little is known, however, about what regulates the expression of PDZ proteins and how the levels of these proteins influence synaptic development. Here, we show that ligands for epidermal growth factor receptors (ErbB1) decrease a particular set of PDZ proteins and negatively influence synaptic formation or maturation. In short-term neocortical cultures, concentrations of epidermal growth factor and amphiregulin (2-9 pM) decreased the expression of glutamate receptor interacting protein 1 (GRIP1) and synapseassociated protein 97 kDa (SAP97) without affecting postsynaptic density-95 (PSD-95) levels and glial proliferation. In long-term cultures, epidermal growth factor treatment resulted in a decrease in the frequency of pan-PDZ-immunoreactive aggregates on dendritic processes. A similar activity on the same PDZ proteins was observed in the developing neocortex following epidermal growth factor administration to rat neonates. Immunoblotting revealed that administered epidermal growth factor from the periphery activated brain ErbB1 receptors and decreased GRIP1 and SAP97 protein levels in the neocortex. Laser-confocal imaging indicated that epidermal growth factor administration suppressed the formation of pan-PDZ-immunoreactive puncta and dispersed those structures in vivo as well. These findings revealed a novel negative activity of ErbB1 receptor ligands that attenuates the expression of the PDZ proteins and inhibits postsynaptic maturation in developing neocortex. KeywordsEGFR; HER1; amphiregulin; synaptic elimination; cerebral cortex; postsynaptic; schizophrenia Proteins carrying PDZ (postsynaptic density-95/discs large/zone occludens-1) domains are referred to as PDZ proteins, which have a modular organization and often function as scaffolding proteins. Recent studies have indicated that these proteins interact with various types of synaptic proteins, such as ion channels, signal transducers, and cytoskeletal thereby playing an important role in the functional localization of these proteins by linking the receptors to the cytoskeleton (Valtschanoff and Weinberg, 2001;Lei et al., 2001;Petersen et al., 2003;Lin et al., 2004). SAP97 binds to AMPARs and similarly modulates their subcellular dynamics (Leonard et al., 1998;Valtschanoff et al., 2000;Wu et al., 2002;Ko et al., 2003). Thus, PDZ proteins perform key roles in synaptic function and plasticity. Little is known, however, about the molecular regulators of PDZ protein expression during synaptic development. Growth factors and neurotrophins, such as brain-derived neurotrophic factor (BDNF) and neuregulin-1 (NRG1), influence synaptic formation and maturation in part by regulating the expression of glutamate and acetylcholine receptors and controlling their subcellular localizations (Ozaki et al., 1997;Narisawa-Saito et al., 19...

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Section: Positive and Negative Regulation Of Pdz Protein Expression Amentioning

confidence: 50%

Section: Positive and Negative Regulation Of Pdz Protein Expression Amentioning

confidence: 99%

ErbB1 receptor ligands attenuate the expression of synaptic scaffolding proteins, GRIP1 and SAP97, in developing neocortex

Yokomaku¹,

Jourdi²,

Kakita³

et al. 2005

Neuroscience

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“…This would require the release of a factor from the sprouted SCG axons near the parasympathetic axons to stimulate their sprouting. Interactions between the sympathetic and parasympathetic systems have been reported previously (Hasan and Smith, 2000;Smith et al, 2002); however, there is no information that sympathetic sprouting can induce parasympathetic sprouting. Furthermore, the rapid loss of the new cholinergic fibers after unilateral ganglionectomy argues against this mechanism because it would require that the adrenergic sympathetic fibers degenerate quickly enough for the parasympathetic fibers to feel the absence of the factor and degenerate, all in the space of 5 d. This is unlikely, because our immunohistochemistry data show that it takes Ͼ3 d, and perhaps as long as 10 d, for central cholinergic fibers to completely degenerate after electrolytic lesion of medial septum.…”

Section: Source Of the Vacht-positive Fibersmentioning

confidence: 98%

Sympathetic Sprouting Drives Hippocampal Cholinergic Reinnervation That Prevents Loss of a Muscarinic Receptor-Dependent Long-Term Depression at CA3–CA1 Synapses

Scheiderer

McCutchen²,

Thacker³

et al. 2006

J. Neurosci.

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Degeneration of septohippocampal cholinergic neurons results in memory deficits attributable to loss of cholinergic modulation of hippocampal synaptic circuits. A remarkable consequence of cholinergic degeneration is the sprouting of noradrenergic sympathetic fibers from the superior cervical ganglia into hippocampus. The functional impact of sympathetic ingrowth on synaptic physiology has never been investigated. Here, we report that, at CA3-CA1 synapses, a Hebbian form of long-term depression (LTD) induced by muscarinic M 1 receptor activation (mLTD) is lost after medial septal lesion. Unexpectedly, expression of mLTD is rescued by sympathetic sprouting. These effects are specific because LTP and other forms of LTD are unaffected. The rescue of mLTD expression is coupled temporally with the reappearance of cholinergic fibers in hippocampus, as assessed by the immunostaining of fibers for VAChT (vesicular acetylcholine transporter). Both the cholinergic reinnervation and mLTD rescue are prevented by bilateral superior cervical ganglionectomy, which also prevents the noradrenergic sympathetic sprouting. The new cholinergic fibers likely originate from the superior cervical ganglia because unilateral ganglionectomy, performed when cholinergic reinnervation is well established, removes the reinnervation on the ipsilateral side. Thus, the temporal coupling of the cholinergic reinnervation with mLTD rescue, together with the absence of reinnervation and mLTD expression after ganglionectomy, demonstrate that the autonomic-driven cholinergic reinnervation is essential for maintaining mLTD after central cholinergic cell death. We have discovered a novel phenomenon whereby the autonomic and central nervous systems experience structural rearrangement to replace lost cholinergic innervation in hippocampus, with the consequence of preserving a form of LTD that would otherwise be lost as a result of cholinergic degeneration.

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“…Figures 1E and 1F show the fluorescence images of SPG neurons that were immunostained with the secondary antibody in the absence of primary AChE (E) and TH (F) antibodies. Images of these negative controls show there is minimal non-specific labeling by Alexa Fluor-488 at the concentration employed.It has been reported that SCG nerve bundles course through the SPG in close proximity to pericaryons [21] and these sympathetic neurons also form synapses with SPG neurons [20]. Thus, SPG neurons were immunostained for the presence of tyrosine hydroxylase, a marker of catecholamine synthesizing neurons.…”

mentioning

confidence: 99%

“…It has been reported that SCG nerve bundles course through the SPG in close proximity to pericaryons [21] and these sympathetic neurons also form synapses with SPG neurons [20]. Thus, SPG neurons were immunostained for the presence of tyrosine hydroxylase, a marker of catecholamine synthesizing neurons.…”

mentioning

confidence: 99%

Electrophysiological and immunofluorescence characterization of Ca2+ channels of acutely isolated rat sphenopalatine ganglion neurons

Margas

Ruiz‐Velasco

2007

Neuroscience Letters

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SummaryThe sphenopalatine ganglion (SPG) is the main parasympathetic ganglion that is involved in regulating cerebral vascular tone and gland secretion. SPG neurons have been implicated in some types of migraine headaches but their precise role has yet to be determined. In addition, very little information is available regarding ion channel modulation by neurotransmitters that are involved in the parasympathetic drive of SPG neurons. In this study, acute isolation of adult rat SPG neurons was developed in order to begin the electrophysiological characterization of this ganglion. Under our dissociation conditions, the average number of neurons obtained per ganglion was greater than 1200.Immunofluorescence imaging results showed positive labeling with acethylcholinesterase (AChE), confirming the parasympathetic nature of SPG neurons. On the other hand, weak tyrosine hydroxylase immunostaining was observed in these neurons. Whole-cell patch-clamp recordings revealed that most of the Ca 2+ current is carried by N-type (53%) and SNX-482 resistant R-type (30%) Ca 2+ channels. In addition, Ca 2+ currents were inhibited in a voltage-dependent manner following exposure to oxotremorine-M (Oxo-M), norepinephrine and ATP via muscarinic acetylcholine receptor 2 (M 2 AChR) subtype, adrenergic and P2Y purinergic receptors, respectively. The peptides VIP and angiotensin II failed to modulate Ca 2+ currents, suggesting that these receptors are not present on the SPG soma or do not couple to Ca 2+ channels. In summary, our data suggest that the Ca 2+ current inhibition mediated by Oxo-M, NE and ATP in adult rat SPG neurons plays an integral part in maintaining parasympathetic control of cranial functions. Keywords sphenopalatine ganglion; parasympathetic; N-type Ca 2+ channels; whole-cell patch-clamp; immunofluorescenceThe sphenopalatine ganglion (SPG) is part of the parasympathetic branch of the autonomic nervous system and is located in the pterygopalatine fossa beneath the maxillary nerve [7]. SPG neurons receive projections from the superior salivatory nucleus and both sympathetic and sensory neurons course through the ganglion as well [7]. SPG neurons innervate the cerebral vasculature, nasal, palatine and lacrimal glands, and thus, regulate cerebral blood flow and secretion from the aforementioned glands [8]. Few electrophysiological studies have been undertaken to examine signaling mechanisms that couple Ca 2+ channels and G protein-coupledCorresponding author: Victor Ruiz-Velasco, Department of Anesthesiology, H187, Penn State College of Medicine, 500 University Drive, Hershey, PA 17033-0850, Phone: 717-531-6076, FAX: 717-531-6221, e-mail: vruizvelasco@psu.edu Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the producti...

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Modulation of parasympathetic neuron phenotype and function by sympathetic innervation

Cited by 22 publications

References 61 publications

ErbB1 receptor ligands attenuate the expression of synaptic scaffolding proteins, GRIP1 and SAP97, in developing neocortex

ErbB1 receptor ligands attenuate the expression of synaptic scaffolding proteins, GRIP1 and SAP97, in developing neocortex

Sympathetic Sprouting Drives Hippocampal Cholinergic Reinnervation That Prevents Loss of a Muscarinic Receptor-Dependent Long-Term Depression at CA3–CA1 Synapses

Electrophysiological and immunofluorescence characterization of Ca2+ channels of acutely isolated rat sphenopalatine ganglion neurons

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